X-ray linear dichroic ptychography

Abstract

Biominerals such as seashells, coral skeletons, bone, and tooth enamel are optically anisotropic crystalline materials with unique nanoscale and microscale organization that translates into exceptional macroscopic mechanical properties, providing inspiration for engineering new and superior biomimetic structures. Using Seriatopora aculeata coral skeleton as a model, here, we experimentally demonstrate X-ray linear dichroic ptychography and map the c-axis orientations of the aragonite (CaCO₃) crystals. Linear dichroic phase imaging at the oxygen K-edge energy shows strong polarization-dependent contrast and reveals the presence of both narrow (<35°) and wide (>35°) c-axis angular spread in the coral samples. These X-ray ptychography results are corroborated by four-dimensional (4D) scanning transmission electron microscopy (STEM) on the same samples. Evidence of co-oriented, but disconnected, corallite subdomains indicates jagged crystal boundaries consistent with formation by amorphous nanoparticle attachment. We expect that the combination of X-ray linear dichroic ptychography and 4D STEM could be an important multimodal tool to study nano-crystallites, interfaces, nucleation, and mineral growth of optically anisotropic materials at multiple length scales.

Keywords: 4D scanning transmission electron microscopy; X-ray linear dichroism; biominerals; coherent diffractive imaging; ptychography.

Fig. 1.

Experimental schematic of X-ray linear dichroic ptychography. (A) Horizontally and vertically polarized X-rays incident on the specimen as spatially overlapping diffraction patterns were acquired below (534.5 eV) and on (536.5 eV) the O K-edge absorption edge to obtain 0° and 90° polarization data. The sample was then rotated 135° and measured again to obtain the 45° and 135° data. The diffraction patterns were directly phased to obtain high-resolution polarization-dependent ptychographic images, from which absorption images were used to compute the PIC maps. (B) Ptychography absorption image of a coral particle used to collect linear dichroic absorption spectra. (C) Experimental XAS spectra of the coral particle at four polarizations, showing the dependence of the CaCO₃ π* peak intensity on the incident X-ray polarization angle. A.u., arbitrary units; OD, optical density.

Fig. 2.

X-ray linear dichroic ptychography of coral-skeleton particles. (A) Ptychography absorption images of three aragonite particles (P1, P2, and P3, from left to right) recorded on the O K-edge absorption resonance at 536.5 eV (Fig. 1C), across four linear polarizations (top to bottom: 0°, 45°, 90°, and 135°), showing strong polarization-dependent absorption contrast and revealing nanoscale morphologies ranging from smooth homogeneous particles several hundred nanometers in size to sub-100-nm fine features. (B) Ptychography phase images of the same particles and polarizations recorded at an energy slightly before O K-edge absorption edge of 534.5 eV (Fig. 1C), showing strong polarization-dependent phase contrast and more edge-sensitive features in internal coral structures.

Fig. 3.

Ptychography PIC map of aragonite coral-skeleton particles. (A) Quantitative PIC maps of the three aragonite particles, calculated using 0°, 45°, and 90° linear dichroic ptychography images. Hue (Upper) denotes in-plane azimuthal crystal c-axis angle (γ) of the crystallite, while brightness (Lower) denotes out-of-plane c-axis angle (χ), all ranging from 0° to 90°. P1 consists of mostly homogeneous orientations, whereas P2 and P3 show more orientational diversity. (B) Histograms of in-plane (γ; Upper) and out-of-plane (χ; Lower) angles for the three particles, showing a narrow γ angular spread (<35°) for P1 and broader spread (>35°) for P2 and P3, suggesting the presence of both spherulitic and randomly oriented submicrometer crystallites at the nanoscopic scale.

Fig. 4.

Diffraction similarity map from 4D STEM with hierarchical clustering. (A) STEM image of particle P3, which was used to acquire scanning electron nano-diffraction patterns. (B) Crystal axis similarity map generated using hierarchical clustering of diffraction patterns. Areas with comparable color resemble subdomains with similar crystal orientations. The resulting map qualitatively agrees with the PIC map generated from ptychography PIC mapping (P3 in Fig. 3). (C) Representative CBED patterns from various regions of the coral particle, colabeled in B and C, showing nanoscale orientational diversity. (Scale bar, 200 nm.) A.u., arbitrary units.